Stutz William E, Bolnick Daniel I
Department of Integrative Biology, University of Texas at Austin, Austin, TX, USA.
Department of Ecology and Evolutionary Biology, University of Colorado at Boulder, Boulder, CO, USA.
Mol Ecol. 2017 Sep;26(18):4772-4786. doi: 10.1111/mec.14158. Epub 2017 May 26.
Major histocompatibility complex (MHC) genes encode proteins that play a central role in vertebrates' adaptive immunity to parasites. MHC loci are among the most polymorphic in vertebrates' genomes, inspiring many studies to identify evolutionary processes driving MHC polymorphism within populations and divergence between populations. Leading hypotheses include balancing selection favouring rare alleles within populations, and spatially divergent selection. These hypotheses do not always produce diagnosably distinct predictions, causing many studies of MHC to yield inconsistent or ambiguous results. We suggest a novel strategy to distinguish balancing vs. divergent selection on MHC, taking advantage of natural admixture between parapatric populations. With divergent selection, individuals with immigrant alleles will be more infected and less fit because they are susceptible to novel parasites in their new habitat. With balancing selection, individuals with locally rare immigrant alleles will be more fit (less infected). We tested these contrasting predictions using three-spine stickleback from three replicate pairs of parapatric lake and stream habitats. We found numerous positive and negative associations between particular MHC IIβ alleles and particular parasite taxa. A few allele-parasite comparisons supported balancing selection, and others supported divergent selection between habitats. But, there was no overall tendency for fish with immigrant MHC alleles to be more or less heavily infected. Instead, locally rare MHC alleles (not necessarily immigrants) were associated with heavier infections. Our results illustrate the complex relationship between MHC IIβ allelic variation and spatially varying multispecies parasite communities: different hypotheses may be concurrently true for different allele-parasite combinations.
主要组织相容性复合体（MHC）基因编码的蛋白质在脊椎动物对寄生虫的适应性免疫中起着核心作用。MHC基因座是脊椎动物基因组中多态性最高的基因座之一，这激发了许多研究来确定驱动种群内MHC多态性以及种群间差异的进化过程。主要假说是平衡选择有利于种群内的稀有等位基因，以及空间上的分歧选择。这些假说并不总是能产生可诊断的明显预测，导致许多关于MHC的研究产生不一致或模糊的结果。我们提出了一种新策略，利用同域分布种群之间的自然混合来区分MHC上的平衡选择和分歧选择。在分歧选择下，携带外来等位基因的个体将更容易受到感染且适应性更差，因为它们易感染新栖息地中的新型寄生虫。在平衡选择下，携带当地稀有外来等位基因的个体将更具适应性（感染更少）。我们使用来自三对重复的同域分布湖泊和溪流栖息地的三刺鱼来检验这些相反的预测。我们发现特定的MHC IIβ等位基因与特定的寄生虫类群之间存在许多正相关和负相关。一些等位基因 - 寄生虫的比较支持平衡选择，而其他的则支持栖息地之间的分歧选择。但是，携带外来MHC等位基因的鱼类并没有总体上更易感染或感染更轻的趋势。相反，当地稀有的MHC等位基因（不一定是外来的）与更严重的感染有关。我们的结果说明了MHC IIβ等位基因变异与空间变化的多物种寄生虫群落之间的复杂关系：对于不同的等位基因 - 寄生虫组合，不同的假说可能同时成立。
